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Journal of Lipid Research, Vol. 50, 2290-2298, November 2009
Copyright © 2009 by American Society for Biochemistry and Molecular Biology

Spatial and temporal alterations of phospholipids determined by mass spectrometry during mouse embryo implantation^[S]

Kristin E. Burnum^*,, Dale S. Cornett^*,, Satu M. Puolitaival^,, Stephen B. Milne^**, David S. Myers^**, Susanne Tranguch, H. Alex Brown^,**, Sudhansu K. Dey^, and Richard M. Caprioli^1,*,,

^* Departments of Biochemistry, Mass Spectrometry Research Center, Nashville, TN 37232
Departments of Biochemistry, Chemistry, Nashville, TN 37232
Departments of Biochemistry, Pharmacology, Nashville, TN 37232
^** Departments of Biochemistry, Pediatrics, Nashville, TN 37232
Departments of Biochemistry, Vanderbilt University Medical Center, Nashville, TN 37232
Division of Reproductive Sciences, Cincinnati Children’s Research Foundation, Cincinnati, OH 45229

¹ To whom correspondence should be addressed. e-mail: r.caprioli{at}vanderbilt.edu

Molecular events involved in successful embryo implantation are not well understood. In this study, we used MALDI imaging mass spectrometry (IMS) technologies to characterize the spatial and temporal distribution of phospholipid species associated with mouse embryo implantation. Molecular images showing phospholipid distribution within implantation sites changed markedly between distinct cellular areas during days 4–8 of pregnancy. For example, by day 8, linoleate- and docosahexaenoate-containing phospholipids localized to regions destined to undergo cell death, whereas oleate-containing phospholipids localized to angiogenic regions. Arachidonate-containing phospholipids showed different segregation patterns depending on the lipid class, revealing a strong correlation of phosphatidylethanolamines and phosphatidylinositols with cytosolic phospholipase A₂ and cyclooxygenase-2 during embryo implantation. LC-ESI-MS/MS was used to validate MALDI IMS phospholipid distribution patterns. Overall, molecular images revealed the dynamic complexity of lipid distributions in early pregnancy, signifying the importance of complex interplay of lipid molecules in uterine biology and implantation.

Supplementary key words imaging mass spectrometry • phosphatidylcholine • sphingomyelins • phosphatidylinositol • phosphatidylserine • phosphatidylglycerol • phosphatidylethanolamine

Abbreviations: AA, arachidonic acid; AM, antimesometrial; COX, cyclooxygenase; cPLA₂, cytosolic PLA₂; DHA, 2,5-dihydroxyacetophenone; DHB, 2,5-dihydroxybenzoic acid; EPC, ectoplacental cone; FTICR, Fourier transform ion cyclotron resonance; IMS, imaging mass spectrometry; LPA, lysophosphatidic acid; M, mesometrial; PC, phosphatidylcholine; PDZ, primary decidual zone; PE, phosphatidylethanolamine; PEp, phosphatidylethanolamine plasmalogen; PG, phosphatidylglycerol; PI, phosphatidylinositol; PS, phosphatidylserine; SDZ, secondary decidual zone; SM, sphingomyelin; TOF, time-of-flight

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